On the issue of screening and prevention of chronic and opportunistic infections in rheumatology
https://doi.org/10.37489/0235-2990-2023-68-1-2-69-76
Abstract
The problem of comorbid infections in rheumatology still remains relevant. Against the background of immunosuppressive/immunomodulatory therapy of immuno-inflammatory rheumatic diseases (IIRD), chronic and opportunistic infections (COI) often develop. Some of these infections can be prevented by performing timely screening procedures and preventive measures. A group of experts from the European Alliance of Rheumatology Associations (EULAR) has prepared recommendations on screening procedures and prevention measures for the most common COI (tuberculosis, chronic viral hepatitis B and C, infections caused by the human immunodeficiency virus and Herpes zoster, pneumocystis pneumonia) within the framework of the IIRD. This article presents the main provisions of this document. The need for periodic review of screening and preventive procedures is emphasized as new scientific data are accumulated.
About the Authors
B. S. BelovRussian Federation
Boris S. Belov — D. Sc. in Medicine, Head of the Laboratory of Comorbid Infections and Vaccine Prevention
Researcher ID: ABD-2219-2020
Scopus Author ID: 7004592537
34А Kashirskoye Highway, Moscow, 115522
Competing Interests:
None
G. I. Gridneva
Russian Federation
Galina I. Gridneva — Ph. D. in Medicine, Researcher at the Laboratory of Comorbid Infections and Vaccine Prevention
ResearcherID: AFN-9929-2022
Scopus Author ID: 56381565500
Moscow
Competing Interests:
None
E. S. Aronova
Russian Federation
Evgenia S. Aronova — Ph. D. in Medicine, Researcher at the Laboratory of Comorbid Infections and Vaccine Prevention
Researcher ID: AAD-1849-2019
Scopus Author ID: 55913403200
Moscow
Competing Interests:
None
N. V. Muravyeva
Russian Federation
Natalia V. Muravyeva — Ph. D. in medicine, Researcher at the Laboratory of Comorbid Infections and Vaccine Prevention
Researcher ID: AAF-4853-2021
Scopus Author ID: 57210263706
Moscow
Competing Interests:
None
References
1. Fragoulis G.E., Dey M., Zhao S. et al. Systematic literature review informing the 2022 EULAR recommendations for screening and prophylaxis of chronic and opportunistic infections in adults with autoimmune in- flammatory rheumatic diseases. RMD Open. 2022; 8 (2): e002726. doi: 10.1136/rmdopen-2022-002726.
2. Fragoulis G.E., Nikiphorou E., Dey M. et al. 2022 EULAR recommendations for screening and prophylaxis of chronic and opportunistic infections in adults with autoimmune inflammatory rheumatic diseases. Ann Rheum Dis. 2022 Nov 3: ard-2022-223335. doi: 10.1136/ard-2022-223335.
3. Long W., Cai F., Wang X., Zheng N., Wu R. High risk of activation of latent tuberculosis infection in rheumatic disease patients. Infect Dis (Lond). 2020; 52 (2): 80–86. doi: 10.1080/23744235.2019.1682187.
4. Jick S.S., Lieberman E.S., Rahman M.U., Choi H.K. Glucocorticoid use, other associated factors, and the risk of tuberculosis. Arthritis Rheum. 2006; 55 (1): 19–26. doi: 10.1002/art.21705.
5. Prevention CfDCa, National Center for HIV/AIDS VH, STD, and TB Prevention, Elimination DoT. Latent tuberculosis infection: A guide for primary health 2020Publication Number 22-0468. URL: https://www.cdc.gov/tb/publications/ltbi/default.htm Access date: 20th January 2023.
6. Ruan Q., Zhang S., Ai J. et al. Screening of latent tuberculosis infection by interferon-γ release assays in rheumatic patients: a systemic review and meta-analysis. Clin Rheumatol. 2016; 35 (2): 417–425. doi: 10.1007/s10067-014-2817-6.
7. Reitblat O., Lerman T.T., Cohen O., Reitblat T. The effect of prednisone on tuberculin skin test reaction in patients with rheumatoid arthritis. Int J Rheumatol. 2018; 2018: 2586916. doi: 10.1155/2018/2586916.
8. Agarwal S., Das S.K., Agarwal G.G., Srivastava R. Steroids decrease prevalence of positive tuberculin skin test in rheumatoid arthritis: implications on anti-TNF Therapies. Interdiscip Perspect Infect Dis. 2014; 2014: 430134. doi: 10.1155/2014/430134.
9. Hsia E.C., Schluger N., Cush J.J. et al. Interferon-γ release assay versus tuberculin skin test prior to treatment with golimumab, a human antitumor necrosis factor antibody, in patients with rheumatoid arthritis, psoriatic arthritis, or ankylosing spondylitis. Arthritis Rheum. 2012; 64 (7): 2068–2077. doi: 10.1002/art.34382.
10. Klein M., Jarosová K., Forejtová S. et al. Quantiferon TB Gold and tuberculin skin tests for the detection of latent tuberculosis infection in patients treated with tumour necrosis factor alpha blocking agents. Clin Exp Rheumatol. 2013; 31 (1): 111–117.
11. Bélard E., Semb S., Ruhwald M. et al. Prednisolone treatment affects the performance of the QuantiFERON gold in-tube test and the tuberculin skin test in patients with autoimmune disorders screened for latent tuberculosis infection. Inflamm Bowel Dis. 2011; 17 (11): 2340–2349. doi: 10.1002/ibd.21605.
12. Soborg B., Ruhwald M., Hetland M.L. et al. Comparison of screening procedures for Mycobacterium tuberculosis infection among patients with inflammatory diseases. J Rheumatol. 2009 Sep; 36 (9): 1876–1884. doi: 10.3899/jrheum.081292.
13. Tamborenea M.N., Tate G., Mysler E. et al. Prevalence of positive ppd in a cohort of rheumatoid arthritis patients. Rheumatol Int. 2010; 30 (5): 613–616. doi: 10.1007/s00296-009-1027-z.
14. Vassilopoulos D., Stamoulis N., Hadziyannis E., Archimandritis A.J. Usefulness of enzyme-linked immunospot assay (Elispot) compared to tuberculin skin testing for latent tuberculosis screening in rheumatic patients scheduled for anti-tumor necrosis factor treatment. J Rheumatol. 2008 Jul; 35 (7): 1271–1276.
15. Arias-Guillén M., Sánchez Menéndez M.M. et al. High rates of tuberculin skin test positivity due to methotrexate therapy: False positive results? Semin Arthritis Rheum. 2018; 48 (3): 538–546. doi: 10.1016/j.semarthrit.2018.03.018.
16. Maeda T., Banno S., Maeda S. et al. Comparison of QuantiFERON-TB Gold and the tuberculin skin test for detecting previous tuberculosis infection evaluated by chest CT findings in Japanese rheumatoid arthritis patients. J Infect Chemother. 2011; 17 (6): 842–848. doi: 10.1007/s10156-011-0250-1.
17. Sargın G., Şentürk T., Ceylan E. et al. TST, QuantiFERON-TB Gold test and T-SPOT.TB test for detecting latent tuberculosis infection in patients with rheumatic disease prior to anti-TNF therapy. Tuberk Toraks. 2018; 66 (2): 136–143. doi: 10.5578/tt.66444.
18. Lee K.H., Jung S.Y., Ha Y.J. et al. Tuberculin reaction is not attenuated in patients with rheumatoid arthritis living in a region with intermediate burden of tuberculosis. Rheumatol Int. 2012; 32 (5): 1421–1424. doi: 10.1007/s00296-011-1889-8.
19. Vassilopoulos D., Tsikrika S., Hatzara C. et al. Comparison of two gamma interferon release assays and tuberculin skin testing for tuberculosis screening in a cohort of patients with rheumatic diseases starting antitumor necrosis factor therapy. Clin Vaccine Immunol. 2011; 18 (12): 2102–2108. doi: 10.1128/CVI.05299-11.
20. Shovman O., Anouk M., Vinnitsky N. et al. QuantiFERON-TB Gold in the identification of latent tuberculosis infection in rheumatoid arthritis: a pilot study. Int J Tuberc Lung Dis. 2009; 13 (11): 1427–1432.
21. Matulis G., Jüni P., Villiger P.M., Gadola S.D. Detection of latent tuberculosis in immunosuppressed patients with autoimmune diseases: performance of a Mycobacterium tuberculosis antigen-specific interferon gamma assay. Ann Rheum Dis. 2008; 67 (1): 84–90. doi: 10.1136/ard.2007.070789.
22. Screening and monitoring of tuberculosis infection in patients receiving immunosuppressive genetically engineered biological drugs. Methodological recommendations No. 133. Moscow: 2018; 33. (in Russian)
23. Bourré-Tessier J., Arino-Torregrosa M., Choquette D. Increased incidence of liver enzymes abnormalities in patients treated with isoniazid in combination with disease modifying and/or biologic agents. Clin Rheumatol. 2014; 33 (8): 1049–1053. doi: 10.1007/s10067-014-2528-z.
24. Vanhoof J., Landewe S., Van Wijngaerden E., Geusens P. High incidence of hepatotoxicity of isoniazid treatment for tuberculosis chemoprophylaxis in patients with rheumatoid arthritis treated with methotrexate or sulfasalazine and anti-tumour necrosis factor inhibitors. Ann Rheum Dis. 2003; 62 (12): 1241–1242. doi: 10.1136/ard.2002.004598.
25. Nam S.H., Oh J.S., Hong S. et al. Early discontinuation of tofacitinib in patients with rheumatoid arthritis co-treated with rifampin for latent tuberculosis. Joint Bone Spine. 2020; 87 (5): 475–479. doi: 10.1016/j.jbspin.2020.04.010.
26. McAllister W.A., Thompson P.J., Al-Habet S.M., Rogers H.J. Rifampicin reduces effectiveness and bioavailability of prednisolone. Br Med J (Clin Res Ed). 1983; 286 (6369): 923–925. doi: 10.1136/bmj.286.6369.923.
27. Myint A., Tong M.J., Beaven S.W. Reactivation of Hepatitis B Virus: A Review of Clinical Guidelines. Clin Liver Dis (Hoboken). 2020; 15 (4): 162–167. doi: 10.1002/cld.883.
28. Mo Y.Q., Liang A.Q., Ma J.D. et al. Discontinuation of antiviral prophylaxis correlates with high prevalence of hepatitis B virus (HBV) reactivation in rheumatoid arthritis patients with HBV carrier state: a real-world clinical practice. BMC Musculoskelet Disord. 2014; 15: 449. doi: 10.1186/1471-2474-15-449.
29. Matsuzaki T., Eguchi K., Nagao N. et al. Hepatitis B virus reactivation in patients with rheumatoid arthritis: A single-center study. Mod Rheumatol. 2018; 28 (5): 808–813. doi: 10.1080/14397595.2017.1419842.
30. Tan J., Zhou J., Zhao P., Wei J. Prospective study of HBV reactivation risk in rheumatoid arthritis patients who received conventional disease-odifying antirheumatic drugs. Clin Rheumatol. 2012 Aug; 31 (8): 1169–1175. doi: 10.1007/s10067-012-1988-2.
31. Kalyoncu U., Emmungil H., Onat A.M. et al. Current antiviral practice and course of Hepatitis B virus infection in inflammatory arthritis: a multicentric observational study (A + HBV study). Eur J Rheumatol. 2015; 2 (4): 149–154. doi: 10.5152/eurjrheum.2015.0111.
32. Chen M.H., Wu C.S., Chen M.H. et al. High Risk of Viral Reactivation in Hepatitis B Patients with Systemic Lupus Erythematosus. Int J Mol Sci. 2021; 22 (17): 9116. doi: 10.3390/ijms22179116.
33. Kalyoncu U., Yonem O., Calguneri M. et al. Prophylactic use of lamivudine with chronic immunosuppressive therapy for rheumatologic disorders. Rheumatol Int. 2009; 29 (7): 777–780. doi: 10.1007/s00296-008-0790-6.
34. Ming-Xu H., Chen M., Cai Y., Yan-Jia H. Clinical outcomes of low-dose leflunomide for rheumatoid arthritis complicated with Hepatitis B virus carriage and safety observation. Pak J Med Sci. 2015; 31 (2): 320–324. doi: 10.12669/pjms.312.6673.
35. Giardina A.R., Ferraro D., Ciccia F. et al. No detection of occult HBV-DNA in patients with various rheumatic diseases treated with anti-TNF agents: a two-year prospective study. Clin Exp Rheumatol. 2013; 31 (1): 25–30.
36. Zingarelli S., Frassi M., Bazzani C. et al. Use of tumor necrosis factoralpha-blocking agents in hepatitis B virus-positive patients: reports of 3 cases and review of the literature. J Rheumatol. 2009; 36 (6): 1188–1194. doi: 10.3899/jrheum.081246.
37. Lan J.L., Chen Y.M., Hsieh T.Y. et al. Kinetics of viral loads and risk of hepatitis B virus reactivation in hepatitis B core antibody-positive rheumatoid arthritis patients undergoing anti-tumour necrosis factor alpha therapy. Ann Rheum Dis. 2011; 70 (10): 1719–1725. doi: 10.1136/ard.2010.148783.
38. Vassilopoulos D., Apostolopoulou A., Hadziyannis E. et al. Long-term safety of anti-TNF treatment in patients with rheumatic diseases and chronic or resolved hepatitis B virus infection. Ann Rheum Dis. 2010; 69 (7): 1352–1355. doi: 10.1136/ard.2009.127233.
39. Chen L.F., Mo Y.Q., Jing J. et al. Short-course tocilizumab increases risk of hepatitis B virus reactivation in patients with rheumatoid arthritis: a prospective clinical observation. Int J Rheum Dis. 2017 Jul; 20 (7): 859–869. doi: 10.1111/1756-185X.13010.
40. Biondo M.I., Germano V., Pietrosanti M. et al. Lack of hepatitis B virus reactivation after anti-tumour necrosis factor treatment in potential occult carriers with chronic inflammatory arthropathies. Eur J Intern Med. 2014; 25 (5): 482–484. doi: 10.1016/j.ejim.2013.11.014.
41. Wang S.T., Tseng C.W., Hsu C.W. et al. Reactivation of hepatitis B virus infection in patients with rheumatoid arthritis receiving tofacitinib. Int J Rheum Dis. 2021; 24 (11): 1362–1369. doi: 10.1111/1756-185X.14217.
42. Kuo M.H., Tseng C.W., Lee C.H. et al. Moderate Risk of Hepatitis B Virus Reactivation in HBsAg-/HBcAb+ Carriers Receiving Rituximab for Rheumatoid Arthritis. Sci Rep. 2020; 10 (1): 2456. doi: 10.1038/s41598-020-59406-4.
43. Tien Y.C., Yen H.H., Chiu Y.M. Incidence and clinical characteristics of hepatitis B virus reactivation in HBsAg-negative/HBcAb-positive patients receiving rituximab for rheumatoid arthritis. Clin Exp Rheumatol. 2017; 35 (5): 831–836.
44. Hwang J.P., Lok A.S. Management of patients with hepatitis B who require immunosuppressive therapy. Nat Rev Gastroenterol Hepatol. 2014; 11 (4): 209–219. doi: 10.1038/nrgastro.2013.216.
45. Chen Y.M., Chen H.H., Huang W.N. et al. Reactivation of hepatitis B virus infection following rituximab treatment in HBsAg-negative, HBcAb-рsitive rheumatoid arthritis patients: A long-term, real-world observation. Int J Rheum Dis. 2019; 22 (6): 1145–1151. doi: 10.1111/1756-185X.13582.
46. Watanabe T., Fukae J., Fukaya S. et al. Incidence and risk factors for reactivation from resolved hepatitis B virus in rheumatoid arthritis patients treated with biological disease-modifying antirheumatic drugs. Int J Rheum Dis. 2019; 22 (4): 574–582. doi: 10.1111/1756-185X.13401.
47. EASL 2017 Recommendations for the treatment of hepatitis B in Russian. URL: https://hcv-forum.ru/viewtopic.php?t=937%20#p4876 Access date: 25th January, 2023
48. Terrault N.A., Lok A.S., McMahon B.J. et al. Update on prevention, diagnosis, and treatment of chronic hepatitis B: AASLD 2018 hepatitis B guidance. Hepatology. 2018; 67 (4): 1560–1599.doi: 10.1002/hep.29800.
49. Brunasso A.M., Puntoni M., Gulia A., Massone C. Safety of anti-tumour necrosis factor agents in patients with chronic hepatitis C infection: a systematic review. Rheumatology. 2011; 50 (9):1700–1711. doi: 10.1093/rheumatology/ker190.
50. Costa L., Caso F., Atteno M. et al. Long-term safety of anti-TNF-α in PsA patients with concomitant HCV infection: a retrospective observational multicenter study on 15 patients. Clin Rheumatol. 2014; 33 (2): 273–276. doi: 10.1007/s10067-013-2378-0.
51. Parke F.A., Reveille J.D. Anti-tumor necrosis factor agents for rheumatoid arthritis in the setting of chronic hepatitis C infection. Arthritis Rheum. 2004; 51 (5): 800–804. doi: 10.1002/art.20702.
52. Peterson J.R., Hsu F.C., Simkin P.A., Wener M.H. Effect of tumour necrosis factor alpha antagonists on serum transaminases and viraemia in patients with rheumatoid arthritis and chronic hepatitis C infection. Ann Rheum Dis. 2003; 62 (11): 1078–1782. doi: 10.1136/ard.62.11.1078.
53. Gandhi N.P., Manadan A.M., Block J.A. Retrospective study of patients on etanercept therapy for rheumatic diseases in patients with chronic hepatitis C virus. J Clin Rheumatol. 2017; 23 (5): 252–257. doi: 10.1097/RHU.0000000000000536.
54. Gridneva G.I., Belov B.S. Current issues in the management of patients with HIV infection and rheumatic diseases. Modern Rheumatology Journal. 2021; 15 (6): 7–12. doi: https://doi.org.10.14412/1996-7012-2021-6-7-12. (in Russian)
55. Cates M., Donati M., Gillet S. et al. Managing varicella zoster virus contact and infection in patients on anti-rheumatic therapy. Rheumatology (Oxford). 2018; 57 (4): 596–605. doi: 10.1093/rheumatology/kex189.
56. Winthrop K.L., Tanaka Y., Lee E.B., Wollenhaupt J., Enizi A., Azevedo V.F., Curtis J.R. Prevention and management of herpes zoster in patients with rheumatoid arthritis and psoriatic arthritis: a clinical review. Clin Exp Rheumatol. 2022; 40 (1): 162–172. doi: 10.55563/clinexprheumatol/cpu6r9.
57. Park J.W., Curtis J.R., Moon J. et al. Prophylactic effect of trimethoprimsulfamethoxazole for pneumocystis pneumonia in patients with rheumatic diseases exposed to prolonged high-dose glucocorticoids. Ann Rheum Dis. 2018; 77 (5): 644–649. doi: 10.1136/annrheumdis-2017-211796.
58. Honda N., Tagashira Y., Kawai S. et al. Reduction of Pneumocystis jirovecii pneumonia and bloodstream infections by trimethoprim-sulfamethoxazole prophylaxis in patients with rheumatic diseases. Scand J Rheumatol. 2021; 50 (5): 365–371. doi: 10.1080/03009742.2020.1850854.
59. Park J.W., Curtis J.R., Kim M.J. et al. Pneumocystis pneumonia in patients with rheumatic diseases receiving prolonged, non-high-dose steroidsclinical implication of primary prophylaxis using trimethoprim-sulfamethoxazole. Arthritis Res Ther. 2019; 21 (1): 207. doi: 10.1186/s13075-019-1996-6.
60. Ogawa J., Harigai M., Nagasaka K. et al. Prediction of and prophylaxis against Pneumocystis pneumonia in patients with connective tissue diseases undergoing medium- or high-dose corticosteroid therapy. Mod Rheumatol. 2005; 15 (2): 91–96. doi: 10.1007/pl00021707.
61. Vananuvat P., Suwannalai P., Sungkanuparph S. et al. Primary prophylaxis for Pneumocystis jirovecii pneumonia in patients with connective tissue diseases. Semin Arthritis Rheum. 2011; 41 (3): 497–502. doi: 10.1016/j.semarthrit.2011.05.004.
62. Teichmann L.L., Woenckhaus M., Vogel C. et al. Fatal Pneumocystis pneumonia following rituximab administration for rheumatoid arthritis. Rheumatology. 2008; 47 (8): 1256–1257. doi: 10.1093/rheumatology/ken234.
63. King C., Harper L., Little M. The complications of vasculitis and its treatment. Best Pract Res Clin Rheumatol. 2018; 32 (1): 125–136. doi: 10.1016/j.berh.2018.07.009.
64. Galli M., Antinori S., Atzeni F. et al. Recommendations for the management of pulmonary fungal infections in patients with rheumatoid arthritis. Clin Exp Rheumatol. 2017; 35 (6): 1018–1028.
65. Sonomoto K., Tanaka H., Nguyen T.M. et al. Prophylaxis against pneumocystis pneumonia in rheumatoid arthritis patients treated with b/tsDMARDs: insights from 3787 cases in the FIRST registry. Rheumatology. 2022; 61 (5): 1831–1840. doi: 10.1093/rheumatology/keab647.
66. Jinno S., Akashi K., Onishi A. et al. Comparative effectiveness of trimethoprim-sulfamethoxazole versus atovaquone for the prophylaxis of pneumocystis pneumonia in patients with connective tissue diseases receiving prolonged high-dose glucocorticoids. Rheumatol Int. 2022; 42 (8): 1403–1409. doi: 10.1007/s00296-021-04945-w.
67. Kitazawa T., Seo K., Yoshino Y. et al. Efficacies of atovaquone, pentamidine, and trimethoprim/sulfamethoxazole for the prevention of Pneumocystis jirovecii pneumonia in patients with connective tissue diseases. J Infect Chemother. 2019; 25 (5): 351–354. doi: 10.1016/j.jiac.2019.01.005.
68. Stamp L.K., Hurst M. Is there a role for consensus guidelines for P. jiroveci pneumonia prophylaxis in immunosuppressed patients with rheumatic diseases? J Rheumatol. 2010; 37 (4): 686–688. doi: 10.3899/jrheum.091426.
Review
For citations:
Belov B.S., Gridneva G.I., Aronova E.S., Muravyeva N.V. On the issue of screening and prevention of chronic and opportunistic infections in rheumatology. Antibiot Khimioter = Antibiotics and Chemotherapy. 2023;68(1-2):69-76. (In Russ.) https://doi.org/10.37489/0235-2990-2023-68-1-2-69-76